Seasonal habitat use and diel vertical migration in female spurdog in Nordic waters

Background Studying habitat use and vertical movement patterns of individual fish over continuous time and space is innately challenging and has therefore largely remained elusive for a wide range of species. Amongst sharks, this applies particularly to smaller-bodied and less wide-ranging species such as the spurdog (Squalus acanthias Linnaeus, 1758), which, despite its importance for fisheries, has received limited attention in biologging and biotelemetry studies, particularly in the North-East Atlantic. Methods To investigate seasonal variations in fine-scale niche use and vertical movement patterns in female spurdog, we used archival data from 19 pregnant individuals that were satellite-tagged for up to 365 days in Norwegian fjords. We estimated the realised niche space with kernel densities and performed continuous wavelet analyses to identify dominant periods in vertical movement. Triaxial acceleration data were used to identify burst events and infer activity patterns. Results Pregnant females frequently utilised shallow depths down to 300 m at temperatures between 8 and 14 °C. Oscillatory vertical moments revealed persistent diel vertical migration (DVM) patterns, with descents at dawn and ascents at dusk. This strict normal DVM behaviour dominated in winter and spring and was associated with higher levels of activity bursts, while in summer and autumn sharks predominantly selected warm waters above the thermocline with only sporadic dive and bursts events. Conclusions The prevalence of normal DVM behaviour in winter months linked with elevated likely foraging-related activity bursts suggests this movement behaviour to be foraging-driven. With lower number of fast starts exhibited in warm waters during the summer and autumn months, habitat use in this season might be rather driven by behavioural thermoregulation, yet other factors may also play a role. Individual and cohort-related variations indicate a complex interplay of movement behaviour and habitat use with the abiotic and biotic environment. Together with ongoing work investigating fine-scale horizontal movement as well as sex- and age-specific differences, this study provides vital information to direct the spatio-temporal distribution of a newly reopened fishery and contributes to an elevated understanding of the movement ecology of spurdog in the North-East Atlantic and beyond. Graphical Abstract Supplementary Information The online version contains supplementary material available at 10.1186/s40462-024-00498-2.


Discussion -Semi-diurnal pattern
A recent study on starry smooth-hound sharks (Mustelus asterias) in the North Sea found semi-diurnal periods to be associated with tidally linked resting behaviour at the bottom (Pohl, 2023).Based on tank experiments suggesting buccal ventilation capabilities in spurdog (Kelly et al., 2020;Skubel et al., 2020), this could be a plausible for spurdog as well.However, for the data presented herein, this semi-diurnal pattern seems unlikely to be indicative of resting behaviour as sharks used variable depths and showed elevated number of fast starts during significant diel patterns.While the maximal tidal range with 1.0-1.5 m (https://sehavniva.no) is rather small in the study region, the northward propagation of the tidal wave along the coast induces internal waves upon entering the fjords, either at the pycnocline between the surface and intermediate layer (~5-10m depth) or the sill level, which in case of the Hardangerfjord is at around 150m depth (Cushman-Roisin and Svendsen, 1983).Fluctuations in the density field associated with internal waves result in a significant vertical displacement of particles such as prey items with a phase corresponding to the astronomical tidal forcing where the semi-diurnal lunar constituent (M2) with a period of 12.42h is the most prominent.Thus, tidal processes are likely affecting the depth use of the sharks as reflected in the semi-diurnal cycles detected in the wavelet analysis.While the co-occurrence of the semi-diurnal with the diurnal cycles might be linked to sharks selecting sill depth during DVM behaviour, the absence of semi-diurnal cycles when sharks spend substantial time above or around the pycnocline in summer, however, leaves some open questions.Rather than a tidal signal, semi-diurnal cycles might be harmonics resulting from non-strictly sinusoidal movement behaviour.This is the case for example when sharks undertake strict DVM with U-shaped dives involving extended periods at a constant depth during day and night with rapid ascents and descents during dusk.Deviations from a sine curve increase during solstice (i.e.long or short photoperiods) and can produce artificial but significant semi-diurnal periods or higher harmonics (see Methods & Results in Detail S2).

Discussion -Hypoxia, offspring predation risk and social avoidance
In addition to temperature, the vertical habitat use and behaviour of sharks has been shown to be affected and limited by low oxygen levels (Nasby-Lucas et al., 2009;Abascal et al., 2011;Sims, 2019;Vedor et al., 2021;Santos et al., 2021).With shallow sills limiting the influx of dense oxygen-rich waters into many of the fjords in the study region (outer sill of Bergen fjord system at 130m, sills to individual fjords often shallower), oxygen levels in the fjord basins are rather low (~2-4 ml/l) (Søvik et al., 2023).The development, persistence, and vertical extent of hypoxic conditions is highly variable between and within fjords, dictated by length, width, depth, orientation as well as the sill depth of the fjord.However, in line with multi-decadal warming, the frequency of such high-density intrusions, commonly occurring in late spring to early summer, has decreased over the past 30 years, leading to decreased fjord basin ventilation (Aksnes et al., 2019;Darelius, 2020;Pitcher et al., 2021).In lab experiments with spurdog, hypoxic conditions have been shown to limit maximum performance (Andres, 2022) and affect physiological processes (Swenson et al., 2005;Zimmer and Wood, 2014), however, implications for habitat selection remain unknown.If oxygen conditions in the deeper water are limiting, which might be amplified due to increasing oxygen demands of developing embryos, sharks might avoid deeper habitats as observed in summer and autumn periods in tagged individuals.
Indication for a deep-water renewal in many fjords on the Norwegian west coast in spring 2021 (Rosland, 2022;Søvik et al., 2023), suggests possible effects to be limited for the subsequent tracking period.Nevertheless, differences in renewal events between years or fjords might contribute to differences between tagging cohorts e.g.2021 and 2022 or contribute to inter-individual variation due to use of different fjord basins.A recent thesis on the vertical distribution on the velvet belly lanternshark (Etmopterus spinax), also displaying DVM behaviour, found no effect on depth use before and after the renewal event in Masfjorden 2021 (Rosland, 2022).Further, the vertical distribution of the common prey species sprat (Sprattus sprattus) was shown to be unaffected by deoxygenation in this system (Kaartvedt et al., 2009).Lab-based choice experiments together with tag-based oxygen measurements and mapping of fine scale horizontal habitat use are needed to assess if the depth use of spurdogs in this system is oxygen-driven or limited.
While we assume the effect of predators in the system to be negligible for mature females given the few limited presence of potential predators in the system for this comparatively large fish (see main paper), predation evasion might play an elevated role during time of parturition (around Nov-Jan) as offspring are more vulnerable and predator naïve.According to the predation-risk hypothesis, female habitat selection might favour offspring security over optimal resource availability (Wearmouth and Sims, 2008).This might explain the lower fast starts at shallower depth in summer and autumn.The lack of higher horizontal resolution, however, does not permit inferences on whether females selected shallow and likely predator poor habitats at the flanks of the fjords or bays or whether they chose surface layers with deeper bathymetry, which would present a rather predation-prone environment.While sporadic dives to mesopelagic depths during summer and autumn might indicate the latter, the steep bathymetry in many of the fjords sets shallow and deep habitats in proximity.Further, locations and depths at which sharks were tagged and recaptured in autumn suggest sharks to have resided in shallower waters along steep drops in bathymetry close to shore at the time point of capture, indicating that sharks may have resided in shallower, more protected habitats during this season.
As habitat use in spurdog is often sexually segregated (Ford, 1921;Shepherd et al., 2002;Stehlink, 2007;Dell'Apa et al., 2014), the prevalence of certain modes of depth use such as DVM or the occupancy of shallow, warm waters might be a result of social avoidance behaviour.In the small-spotted catshark, for example, females hide in shallow waters to avoid males that dominate in deeper waters (Sims et al., 2001;Sims, 2006).As this study focussed on mature, pregnant females, inferences about the contribution of avoidance behaviour remain beyond the scope of this paper.

Supplementary Table
Table S1: Tagging information for all PSAT tagged female spurdogs.This includes tag ID, dates of tagging and surfacing due to programmed pop-off, early tag detachment or shark recapture (DATEon, DATEoff), total length (TL), coordinates of tagging and surfacing locations (LOCon, LOCoff), the reason for track termination and the number of days at liberty (DAYS) and those days used for analysis (DAYS used).PD denotes premature detachment.

Figure S1 :
Figure S1: Tagging (circles) and pop-up sites (triangles) of PSATs from 19 female spurdogs deployed in autumn 2019 to 2022 along the southwestern Norwegian coast.Note that tagging locations in 2021 and 2022 were identical.Numbers associated with pop-up sites (triangles) indicate respective shark IDs.Note that colours represent tagging year, respective pop-ups occurred in the consecutive year.Bathymetry and elevation contours are shown every 100m.

Figure S2 :
Figure S2: Depth-timeseries for recapture events for sharks 9, 11, and 17.Data are based on 1-minute interval median depths, colours indicate tagging cohort association.Grey polygons mark night defined by sunset and sunrise and nautical dusk and dawn (sun 12° below horizon, winter only) around the tagging location.

Figure S2 :
Figure S2: Activity seascapes for each month based on 5-sec resolution PSAT data with fast starts calculated using a (A) 97% and (B) 99% MA threshold.Data are aggregated by month in 10m depth bins and hour of day.Dotted vertical lines mark the median hour of sunrise and sunset for a given month.

Figure S4 :
Figure S4: Time-at-depth (A) and time-at-temperature (B) histograms for the entire deployment.Bars represent mean percentage of time (summarised by date) spent across individuals in each of the twelve depth and eight temperature bins.The means were weighted by the reciprocal of data points per Julian day to account for the heterogenic temporal coverage due to different deployment lengths.Error bars indicate standard errors.

Figure S5 :
Figure S5: Average daily depth (A) and temperature (B) use across the different months of deployment based on 1-minute interval median depth and temperature values.Boxplots show the average median, boxes indicate the interquartile range (IQR -25 and 75% quartiles) and whiskers extent to the average daily minimum and maximum depth and temperature per month.

Figure S3 :
Figure S3: Realised depth-temperature niche by female spurdogs in the context of available habitat for each month.Number of sharks contributing to each monthly plot are indicated.Red colours denote the density of hourly datapoints within a given grid cell.Black dotted and solid lines indicate the niche space that encompasses 50% and 95% of these data, respectively.The profiles in blue are CTD profiles from the hydrographic station H2 in Hardangerfjord with the mean and corresponding standard errors shown for every meter down to 250m in the given month.For visualisation purposes, the y-axis was limited to 400m depth.

Figure S7 :
Figure S7: Time-at-depth histograms for each month of tag attachment.Bars represent mean percentage of time (summarised by date) spent across individuals in each of the twelve defined depth ranges, with error bars indicating standard errors.Number of sharks contributing to each monthly plot are indicated.

Figure S8 :
Figure S8: Time-at-temperature histograms for each month of tag attachment.Bars represent mean percentage of time (summarised by date) spent across individuals in each of the eight defined temperature ranges, with error bars indicating standard errors.Number of sharks contributing to each monthly plot are indicated.

Figure S4 :
Figure S4: Vertical habitat use across deployment period for each shark.(A) Hourly median depth timeseries and with colour coded temperatures.The upper bar indicates the presence (dark grey) or absence (light grey) of diel vertical migration (DVM) behaviour, based on significance (p≤0.05) of wavelet powers at 24h. (B) Wavelet scalogram based on median hourly depth.Significant powers (p ≤0.05) are highlighted with grey contours.(C-G)Actograms for 1-minute interval median depth (C), temperature (D), and light level (E) use, hourly vertical speed (E), and hourly cumulated fast starts (F) across the time of day.In (D) red colours mark descents, while blue colours represent ascents.Solid lines indicate times of sunrise and sunset, dashed lines nautical dusk and dawn associated with the tagging location.Note the different date ranges between sharks on the x-axis.A description of how light levelscorrespond to light intensity is provided in Detail S1.

Figure S10 :
Figure S10: Hourly median depth used across all individuals for a given month.Medians and 25, 75% confidence intervals are shown.Number of sharks contributing to each monthly plot are indicated.

Figure S5 :
Figure S5: Inter-individual differences in median depth distributions for day and night during as significant classified diel vertical migration (DVM).Results from a Wilcoxon signed rank test shown for each shark.Violin plots in grey represent the full distribution of the data.Boxplots show median and lower and upper quartiles with whiskers extending to 1.5*IQR.

Figure S12 :
Figure S12: Vertical occupancy (A) and activity (B) landscapes for each month based on 5-sec resolution PSAT data with the first 24h after tagging removed (as in all other analysis).Data are aggregated by month in 10m depth bins and hour of day.The number of data points per month by which data was scaled is noted in brackets.(A) Occupancy calculated as the number of data points within each depth-time cell divided by the number of data points within the respective month.(B) Activity calculated as the proportion of fast starts within each depth-time cell divided by the number of data points per month.Dotted vertical lines mark the median hour of sunrise and sunset for a given month.

Figure S6 :
Figure S6: Cumulated hourly fast starts based on all individuals and time periods for diel vertical migration (DVM) and non-DVM behaviour.Violin plots in grey represent the full distribution of the data.Boxplot show median and lower and upper quartiles with whiskers extending to 1.5*IQR.

Figure S7 :
Figure S7: Median hourly number of fast starts paired for each day and night per individual (A) for as significant diel vertical migration (DVM) classified behaviour and (B) as non-DVM classified behaviour.Violin plots in grey represent the full distribution of the data.Boxplot show median and lower and upper quartiles with whiskers extending to 1.5*IQR.

Figure S8 :
Figure S8: Inter-individual differences in median hourly cumulated fast start distributions for day and night.Results from a Wilcoxon signed rank test are shown for each individual shark.Violin plots in grey represent the full distribution of the data.Boxplot show median and lower and upper quartiles with whiskers extending to 1.5*IQR.

Figure S9 :
Figure S9: Differences in hourly cumulated fast starts per months for shark11,12,14,15,17,18, and 19  which covered a minimum of 320 days.The red dashed line marks the population median (8 fast starts) of the seven individuals across months.The y-axis was limited to 200m for visualisation purposes.Violin plots in grey represent the full distribution of the data.Boxplot show median and lower and upper quartiles with whiskers extending to 1.5*IQR.

Figure S10 :
Figure S10: Environmental relationships of light level (A), temperature (B) and depth (C) on the median hourly number of fast starts.Medians of fast starts were taken across bins of 1 light level unit, 0.1°C, and 10m respectively.Bins with n<100 are disregarded.Red line marks a fitted loess function with span = 0.75.95% confidence intervals shown in grey.A description of how light levels correspond to light intensity is provided in Detail S1.

Figure S11 :
Figure S11: Vertical occupancy (A) and activity (B) landscapes for each month based on 5-sec resolution PSAT data with the first 120h (5 days) after tagging removed.Data are aggregated by month in 10m depth bins and hour of day.The number of data points per month by which data was scaled is noted in brackets.(A) Vertical occupancy calculated as the number of data points within each depth-time cell divided by the number of data points within the respective month.(B) Activity calculated as the proportion of fast starts within each depth-time cell divided by the number of data points per month.Dotted vertical lines mark the median hour of sunrise and sunset for a given month.

Figure S19 :
Figure S19: Scalograms obtained from a continuous wavelet analysis with equivalent parameters as used in the main analysis on three synthetic hourly depth time series for fictive 180 days mimicking simplified strict diel vertical movement patterns, alternating between 80 and 200 m depth.Scalogram resulting (A) from a 12:12h pattern, comparable to situations during equinox, (B) from a 6:18h pattern, and (C) from a 3:21h pattern, comparable to daynight patterns during solstice in the study area.